Although the one-cell zygote has a large complement of mRNAs synthesized during oogenesis, the extent to which these maternal genes modulate early development is unknown. We have focused our investigations on understanding the molecular details of oocyte-specific genes and have chosen as our model system the genes that code for three sulfated glycoproteins of the mouse zona pellucida (ZP-1, ZP-2, and ZP-3). We have isolated cDNAs coding for ZP-3, the mouse sperm receptor, from an ovarian cDNA library cloned in the Lambdagt-11 expression vector. The identity of these clones was confirmed by a comparison of their nucleic acid sequence with the amino acid sequence of the ZP-3 protein. We have shown that the ZP-3 message is expressed as a 1.6 kb poly-adenlyated mRNA which is found uniquely in ovarian tissue. Furthermore, from Northern analysis and in situ hybridizations, it appears that ZP-3 is expressed only in oocytes and not in surrounding granulosa cells. Based on our in situ data, the gene does not appear to be transcribed in resting oocytes (17 Mum) but rapidly becomes a very abundant message in growing oocytes (50 Mum before being turned off in fully grown oocytes (70 Mum). Thus, the transcription of the gene appears to closely parallel our previous obsrevations on zona protein biosynthesis during oogenesis. Somatic cell hybrids were used to localize the ZP-3 locus to mouse chromosome 6 where it appears to exist as a single copy gene. Although the structure of the gene is the same in germ-line and somatic tissues, the ZP-3 gene is hypomethylated in ovarian tissue (where it is expressed) compared to somatic tissue.